Role of FoxO1 in regulating autophagy in type 2 diabetes mellitus (Review)
- Authors:
- Xiudan Li
- Tingting Wan
- Yanbo Li
-
Affiliations: Department of Endocrinology, First Affiliated Hospital of Harbin Medical University, Harbin, Heilongjiang 150001, P.R. China - Published online on: May 2, 2021 https://doi.org/10.3892/etm.2021.10139
- Article Number: 707
-
Copyright: © Li et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Harris SR, Carrillo M and Fujioka K: Binge-eating disorder and type 2 diabetes: A Review. Endocr Pract: December 20, 2020. doi: 10.1016/j.eprac.2020.10.005. | |
Wang Y, Li YB, Yin JJ, Wang Y, Zhu LB, Xie GY and Pan SH: Autophagy regulates inflammation following oxidative injury in diabetes. Autophagy. 9:272–277. 2013.PubMed/NCBI View Article : Google Scholar | |
Chen ZF, Li YB, Han JY, Yin JJ, Wang Y, Zhu LB and Xie GY: Liraglutide prevents high glucose level induced insulinoma cells apoptosis by targeting autophagy. Chin Med J (Engl). 126:937–941. 2013.PubMed/NCBI | |
Zhu LB, Cao MM, Wang J, Su Y, Jiang W, Liu GD and Li YB: Role of autophagy in LPS-induced inflammation in INS-1 cells. Mol Med Rep. 19:5211–5218. 2019.PubMed/NCBI View Article : Google Scholar | |
Fan M, Jiang H, Zhang Y, Ma Y, Li L and Wu J: Liraglutide enhances autophagy and promotes pancreatic β cell proliferation to ameliorate type 2 diabetes in high-fat-fed and streptozotocin-treated mice. Med Sci Monit. 24:2310–2316. 2018.PubMed/NCBI View Article : Google Scholar | |
Melmed L, Polonsky KS, Reed Larsen P and Kronenberg H: Chapter on pathogenesis of type 2 diabetes-Williams Textbook of Endocrinology. 13th edition. Elsevier, 2016. | |
Zhang N, Cao MM, Liu H, Xie GY and Li YB: Autophagy regulates insulin resistance following endoplasmic reticulum stress in diabetes. J Physiol Biochem. 71:319–327. 2015.PubMed/NCBI View Article : Google Scholar | |
Li Q, Jia S, Xu L, Li B and Chen N: Metformin-induced autophagy and irisin improves INS-1 cell function and survival in high-glucose environment via AMPK/SIRT1/PGC-1α signal pathway. Food Sci Nutr. 7:1695–1703. 2019.PubMed/NCBI View Article : Google Scholar | |
Cheng STW, Li SYT and Leung PS: Fibroblast growth factor 21 stimulates pancreatic islet autophagy via inhibition of AMPK-mTOR signaling. Int J Mol Sci 20: 2517. doi: 10.3390/ijms20102517. | |
Lee YH, Kim J, Park K and Lee MS: β-cell autophagy: Mechanism and role in β-cell dysfunction. Mol Metab. 27S:S92–S103. 2019.PubMed/NCBI View Article : Google Scholar | |
Wu Q, Hu Y, Jiang M, Wang F and Gong G: Effect of autophagy regulated by Sirt1/FoxO1 pathway on the release of factors promoting thrombosis from vascular endothelial cells. Int J Mol Sci. 20(4132)2019.PubMed/NCBI View Article : Google Scholar : doi: 10.3390/ijms20174132. | |
He W, Zhang A, Qi L, Na C, Jiang R, Fan Z and Chen J: FOXO1, a potential therapeutic target, regulates autophagic Flux, oxidative stress, mitochondrial dysfunction, and apoptosis in human cholangiocarcinoma QBC939 cells. Cell Physiol Biochem. 45:1506–1514. 2018.PubMed/NCBI View Article : Google Scholar | |
Kitamura T: The role of FOXO1 in β-cell failure and type 2 diabetes mellitus. Nat Rev Endocrinol. 9:615–623. 2013.PubMed/NCBI View Article : Google Scholar | |
Xing YQ, Li A, Yang Y, Li XX, Zhang LN and Guo HC: The regulation of FOXO1 and its role in disease progression. Life Sci. 193:124–131. 2018.PubMed/NCBI View Article : Google Scholar | |
Cheng Z: The FoxO-autophagy axis in health and disease. Trends Endocrinol Metab. 30:658–671. 2019.PubMed/NCBI View Article : Google Scholar | |
Chen B, Zhou W, Zhao W, Yuan P, Tang C, Wang G, Leng J, Ma J, Wang X, Hui Y, et al: Oxaliplatin reverses the GLP-1R-mediated promotion of intrahepatic cholangiocarcinoma by altering FoxO1 signaling. Oncol Lett. 18:1989–1998. 2019.PubMed/NCBI View Article : Google Scholar | |
Kamei Y, Miura S, Suzuki M, et al: Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated Type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem. 2004;279(39):41114‐41123. doi:10.1074/jbc.M400674200. | |
Nakae J, Cao Y, Oki M, et al: Forkhead transcription factor FoxO1 in adipose tissue regulates energy storage and expenditure. Diabetes. 2008;57(3):563‐576. doi:10.2337/db07-0698. | |
Gu L, Ding X, Wang Y, et al: Spexin alleviates insulin resistance and inhibits hepatic gluconeogenesis via the FoxO1/PGC-1α pathway in high-fat-diet-induced rats and insulin resistant cells. Int J Biol Sci. 2019;15(13):2815‐2829. Published 2019 Nov 1. doi:10.7150/ijbs.31781. | |
Kitamura YI, Kitamura T, Kruse JP, Raum JC, Stein R, Gu W and Accili D: FoxO1 protects against pancreatic beta cell failure through NeuroD and MafA induction. Cell Metab. 2:153–163. 2005.PubMed/NCBI View Article : Google Scholar | |
Kobayashi M, Kikuchi O, Sasaki T, Kim HJ, Yokota-Hashimoto H, Lee YS, Amano K, Kitazumi T, Susanti VY, Kitamura YI, et al: FoxO1 as a double-edged sword in the pancreas: Analysis of pancreas- and β-cell-specific FoxO1 knockout mice. Am J Physiol Endocrinol Metab. 302:E603–E613. 2012.PubMed/NCBI View Article : Google Scholar | |
Gerst F, Kaiser G, Panse M, Sartorius T, Pujol A, Hennige AM, Machicao F, Lammers R, Bosch F, Häring HU, et al: Protein kinase Cδ regulates nuclear export of FOXO1 through phosphorylation of the chaperone 14-3-3ζ. Diabetologia. 58:2819–2831. 2015.PubMed/NCBI View Article : Google Scholar | |
Kaiser G, Gerst F, Michael D, Berchtold S, Friedrich B, Strutz-Seebohm N, Lang F, Häring HU and Ullrich S: Regulation of forkhead box O1 (FOXO1) by protein kinase B and glucocorticoids: Different mechanisms of induction of beta cell death in vitro. Diabetologia. 56:1587–1595. 2013.PubMed/NCBI View Article : Google Scholar | |
Kitamura T, Nakae J, Kitamura Y, Kido Y, Biggs WH III, Wright CV, White MF, Arden KC and Accili D: The forkhead transcription factor Foxo1 links insulin signaling to Pdx1 regulation of pancreatic beta cell growth. J Clin Invest. 110:1839–1847. 2002.PubMed/NCBI View Article : Google Scholar | |
Mo X, Wang X, Ge Q and Bian F: The effects of SIRT1/FoxO1 on LPS induced INS-1 cells dysfunction. Stress. 22:70–82. 2019.PubMed/NCBI View Article : Google Scholar | |
Boughanem H, Cabrera-Mulero A, Millán-Gómez M, Garrido-Sánchez L, Cardona F, Tinahones FJ, Moreno-Santos I and Macías-González M: Transcriptional analysis of FOXO1, C/EBP-α and PPAR-γ2 genes and their association with obesity-related insulin resistance. Genes. 10(706)2019.PubMed/NCBI View Article : Google Scholar : doi.org/10.3390/genes10090706. | |
Samuel VT, Choi CS, Phillips TG, Romanelli AJ, Geisler JG, Bhanot S, McKay R, Monia B, Shutter JR, Lindberg RA, et al: Targeting foxo1 in mice using antisense oligonucleotide improves hepatic and peripheral insulin action. Diabetes. 55:2042–2050. 2006.PubMed/NCBI View Article : Google Scholar | |
Yang L, Li P, Fu S, Calay ES and Hotamisligil GS: Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab. 11:467–478. 2010.PubMed/NCBI View Article : Google Scholar | |
Rivera JF, Costes S, Gurlo T, Glabe CG and Butler PC: Autophagy defends pancreatic β cells from human islet amyloid polypeptide-induced toxicity. J Clin Invest. 124:3489–3500. 2014.PubMed/NCBI View Article : Google Scholar | |
Quan W, Hur KY, Lim Y, Oh SH, Lee JC, Kim KH, Kim GH, Kim SW, Kim HL, Lee MK, et al: Autophagy deficiency in beta cells leads to compromised unfolded protein response and progression from obesity to diabetes in mice. Diabetologia. 55:392–403. 2012.PubMed/NCBI View Article : Google Scholar | |
Bachar-Wikstrom E, Wikstrom JD, Ariav Y, Tirosh B, Kaiser N, Cerasi E and Leibowitz G: Stimulation of autophagy improves endoplasmic reticulum stress-induced diabetes. Diabetes. 62:1227–1237. 2013.PubMed/NCBI View Article : Google Scholar | |
Riahi Y, Wikstrom JD, Bachar-Wikstrom E, Polin N, Zucker H, Lee MS, Quan W, Haataja L, Liu M, Arvan P, et al: Erratum to: Autophagy is a major regulator of beta cell insulin homeostasis. Diabetologia. 59:1575–1576. 2016.PubMed/NCBI View Article : Google Scholar | |
Yin JJ, Li YB, Wang Y, Liu GD, Wang J, Zhu XO and Pan SH: The role of autophagy in endoplasmic reticulum stress-induced pancreatic β cell death. Autophagy. 8:158–164. 2012.PubMed/NCBI View Article : Google Scholar | |
Priyadarshini M, Cole C, Oroskar G, Ludvik AE, Wicksteed B, He C and Layden BT: Free fatty acid receptor 3 differentially contributes to β-cell compensation under high-fat diet and streptozotocin stress. Am J Physiol Regul Integr Comp Physiol. 318:R691–R700. 2020.PubMed/NCBI View Article : Google Scholar | |
Huang C, Wang HY, Wang ME, Hsu MC, Wu YS, Jiang YF, Wu LS, Jong DS and Chiu CH: Kisspeptin-activated autophagy independently suppresses non-glucose-stimulated insulin secretion from pancreatic β-cells. Sci Rep. 9(17451)2019.PubMed/NCBI View Article : Google Scholar | |
Zhou J, Kang X, Luo Y, Yuan Y, Wu Y, Wang M and Liu D: Glibenclamide-induced autophagy inhibits its insulin secretion-improving function in β cells. Int J Endocrinol. 2019(1265175)2019.PubMed/NCBI View Article : Google Scholar : doi.org/10.1155/2019/1265175. | |
Yamamoto S, Kuramoto K, Wang N, Situ X, Priyadarshini M, Zhang W, Cordoba-Chacon J, Layden BT and He C: Autophagy differentially regulates insulin production and insulin sensitivity. Cell Rep. 23:3286–3299. 2018.PubMed/NCBI View Article : Google Scholar | |
Ebato C, Uchida T, Arakawa M, Komatsu M, Ueno T, Komiya K, Azuma K, Hirose T, Tanaka K, Kominami E, et al: Autophagy is important in islet homeostasis and compensatory increase of beta cell mass in response to high-fat diet. Cell Metab. 8:325–332. 2008.PubMed/NCBI View Article : Google Scholar | |
Jung HS, Chung KW, Won Kim J, Kim J, Komatsu M, Tanaka K, Nguyen YH, Kang TM, Yoon KH, Kim JW, et al: Loss of autophagy diminishes pancreatic beta cell mass and function with resultant hyperglycemia. Cell Metab. 8:318–324. 2008.PubMed/NCBI View Article : Google Scholar | |
Galicia-Garcia U, Benito-Vicente A, Jebari S, Larrea-Sebal A, Siddiqi H, Uribe KB, Ostolaza H and Martín C: Pathophysiology of type 2 diabetes mellitus. Int J Mol Sci. 21(21)2020.PubMed/NCBI View Article : Google Scholar | |
Frendo-Cumbo S, Jaldin-Fincati JR, Coyaud E, Laurent EMN, Townsend LK, Tan JMJ, Xavier RJ, Pillon NJ, Raught B, Wright DC, et al: Deficiency of the autophagy gene ATG16L1 induces insulin resistance through KLHL9/KLHL13/CUL3-mediated IRS1 degradation. J Biol Chem. 294:16172–16185. 2019.PubMed/NCBI View Article : Google Scholar | |
Chan YK, Sung HK, Jahng JW, Kim GH, Han M and Sweeney G: Lipocalin-2 inhibits autophagy and induces insulin resistance in H9c2 cells. Mol Cell Endocrinol. 430:68–76. 2016.PubMed/NCBI View Article : Google Scholar | |
Guo Q, Xu L, Li H, Sun H, Liu J, Wu S and Zhou B: Progranulin causes adipose insulin resistance via increased autophagy resulting from activated oxidative stress and endoplasmic reticulum stress. Lipids Health Dis. 16(25)2017.PubMed/NCBI View Article : Google Scholar : doi.org/10.1186/s12944-017-0425-6. | |
Barlow AD and Thomas DC: Autophagy in diabetes: Β-cell dysfunction, insulin resistance, and complications. DNA Cell Biol. 34:252–260. 2015.PubMed/NCBI View Article : Google Scholar | |
Chen ZF, Li YB, Han JY, Wang J, Yin JJ, Li JB and Tian H: The double-edged effect of autophagy in pancreatic beta cells and diabetes. Autophagy. 7:12–16. 2011.PubMed/NCBI View Article : Google Scholar | |
Buteau J and Accili D: Regulation of pancreatic beta-cell function by the forkhead protein FoxO1. Diabetes Obes Metab. 9 (Suppl 2):140–146. 2007.PubMed/NCBI View Article : Google Scholar | |
Kitamura T and Ido Kitamura Y: Role of FoxO proteins in pancreatic beta cells. Endocr J. 54:507–515. 2007.PubMed/NCBI View Article : Google Scholar | |
Talchai SC and Accili D: Legacy effect of Foxo1 in pancreatic endocrine progenitors on adult β-cell mass and function. Diabetes. 64:2868–2879. 2015.PubMed/NCBI View Article : Google Scholar | |
Cai H, Jiang Z, Yang X, Lin J, Cai Q and Li X: Circular RNA HIPK3 contributes to hyperglycemia and insulin homeostasis by sponging miR-192-5p and upregulating transcription factor forkhead box O1. Endocr J. 67:397–408. 2020.PubMed/NCBI View Article : Google Scholar | |
Robertson RP, Harmon J, Tran PO, Tanaka Y and Takahashi H: Glucose toxicity in beta-cells: Type 2 diabetes, good radicals gone bad, and the glutathione connection. Diabetes. 52:581–587. 2003.PubMed/NCBI View Article : Google Scholar | |
Zhang T, Kim DH, Xiao X, Lee S, Gong Z, Muzumdar R, Calabuig-Navarro V, Yamauchi J, Harashima H, Wang R, et al: FoxO1 plays an important role in regulating β-cell compensation for insulin resistance in male mice. Endocrinology. 157:1055–1070. 2016.PubMed/NCBI View Article : Google Scholar | |
Kibbe C, Chen J, Xu G, Jing G and Shalev A: FOXO1 competes with carbohydrate response element-binding protein (ChREBP) and inhibits thioredoxin-interacting protein (TXNIP) transcription in pancreatic beta cells. J Biol Chem. 288:23194–23202. 2013.PubMed/NCBI View Article : Google Scholar | |
Kim HJ, Kobayashi M, Sasaki T, Kikuchi O, Amano K, Kitazumi T, Lee YS, Yokota-Hashimoto H, Susanti VY, Kitamura YI, et al: Overexpression of FoxO1 in the hypothalamus and pancreas causes obesity and glucose intolerance. Endocrinology. 153:659–671. 2012.PubMed/NCBI View Article : Google Scholar | |
Zhang X, Yong W, Lv J, Zhu Y, Zhang J, Chen F, Zhang R, Yang T, Sun Y and Han X: Inhibition of forkhead box O1 protects pancreatic beta-cells against dexamethasone-induced dysfunction. Endocrinology. 150:4065–4073. 2009.PubMed/NCBI View Article : Google Scholar | |
Kong X, Zhang L, Hua X and Ma X: Squamosamide derivative FLZ protects pancreatic β-cells from glucotoxicity by stimulating Akt-FOXO1 pathway. J Diabetes Res. 2015(803986)2015.PubMed/NCBI View Article : Google Scholar | |
Liu XD, Ruan JX, Xia JH, Yang SL, Fan JH and Li K: The study of regulatory effects of Pdx-1, MafA and NeuroD1 on the activity of porcine insulin promoter and the expression of human islet amyloid polypeptide. Mol Cell Biochem. 394:59–66. 2014.PubMed/NCBI View Article : Google Scholar | |
Shao S, Liu Z, Yang Y, Zhang M and Yu X: SREBP-1c, Pdx-1, and GLP-1R involved in palmitate-EPA regulated glucose-stimulated insulin secretion in INS-1 cells. J Cell Biochem. 111:634–642. 2010.PubMed/NCBI View Article : Google Scholar | |
Zhang F, Ma D, Zhao W, Wang D, Liu T, Liu Y, Yang Y, Liu Y, Mu J, Li B, et al: Obesity-induced overexpression of miR-802 impairs insulin transcription and secretion. Nat Commun. 11(1822)2020.PubMed/NCBI View Article : Google Scholar : doi: 10.1038/s41467-020-15529-w. | |
Kim DH, Zhang T, Ringquist S and Dong HH: Targeting FoxO1 for hypertriglyceridemia. Curr Drug Targets. 12:1245–1255. 2011.PubMed/NCBI View Article : Google Scholar | |
Matsumoto M, Han S, Kitamura T and Accili D: Dual role of transcription factor FoxO1 in controlling hepatic insulin sensitivity and lipid metabolism. J Clin Invest. 116:2464–2472. 2006.PubMed/NCBI View Article : Google Scholar | |
Wang S, Ai H, Liu L, Zhang X, Gao F, Zheng L, Yi J, Sun L, Yu C, Zhao H, et al: Micro-RNA-27a/b negatively regulates hepatic gluconeogenesis by targeting FOXO1. Am J Physiol Endocrinol Metab. 317:E911–E924. 2019.PubMed/NCBI View Article : Google Scholar | |
Penniman CM, Suarez Beltran PA, Bhardwaj G, Junck TL, Jena J, Poro K, Hirshman MF, Goodyear LJ and O'Neill BT: Loss of FoxOs in muscle reveals sex-based differences in insulin sensitivity but mitigates diet-induced obesity. Mol Metab. 30:203–220. 2019.PubMed/NCBI View Article : Google Scholar | |
Zhang W, Patil S, Chauhan B, Guo S, Powell DR, Le J, Klotsas A, Matika R, Xiao X, Franks R, et al: FoxO1 regulates multiple metabolic pathways in the liver: Effects on gluconeogenic, glycolytic, and lipogenic gene expression. J Biol Chem. 281:10105–10117. 2006.PubMed/NCBI View Article : Google Scholar | |
Zhang K, Li L, Qi Y, Zhu X, Gan B, DePinho RA, Averitt T and Guo S: Hepatic suppression of Foxo1 and Foxo3 causes hypoglycemia and hyperlipidemia in mice. Endocrinology. 153:631–646. 2012.PubMed/NCBI View Article : Google Scholar | |
Du K, Herzig S, Kulkarni RN and Montminy M: TRB3: A tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science. 300:1574–1577. 2003.PubMed/NCBI View Article : Google Scholar | |
Greer EL, Oskoui PR, Banko MR, Maniar JM, Gygi MP, Gygi SP and Brunet A: The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem. 282:30107–30119. 2007.PubMed/NCBI View Article : Google Scholar | |
Caselli C: Role of adiponectin system in insulin resistance. Mol Genet Metab. 113:155–160. 2014.PubMed/NCBI View Article : Google Scholar | |
Yaghootkar H, Lamina C, Scott RA, Dastani Z, Hivert MF, Warren LL, Stancáková A, Buxbaum SG, Lyytikäinen LP, Henneman P, et al: GENESIS Consortium; RISC Consortium: Mendelian randomization studies do not support a causal role for reduced circulating adiponectin levels in insulin resistance and type 2 diabetes. Diabetes. 62:3589–3598. 2013.PubMed/NCBI View Article : Google Scholar | |
Wang A, Li T, An P, Yan W, Zheng H, Wang B and Mu Y: Exendin-4 upregulates adiponectin level in adipocytes via Sirt1/Foxo-1 signaling pathway. PLoS One. 12(e0169469)2017.PubMed/NCBI View Article : Google Scholar | |
Sanchez AM, Bernardi H, Py G and Candau RB: Autophagy is essential to support skeletal muscle plasticity in response to endurance exercise. Am J Physiol Regul Integr Comp Physiol. 307:R956–R969. 2014.PubMed/NCBI View Article : Google Scholar | |
Jash S and Puri V: FoxO1-autophagy axis regulates lipid droplet growth via FSP27. Cell Cycle. 15:2856–2857. 2016.PubMed/NCBI View Article : Google Scholar | |
Zhao Y, Yang J, Liao W, Liu X, Zhang H, Wang S, Wang D, Feng J, Yu L and Zhu WG: Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity. Nat Cell Biol. 12:665–675. 2010.PubMed/NCBI View Article : Google Scholar | |
Liu L, Zheng LD, Zou P, Brooke J, Smith C, Long YC, Almeida FA, Liu D and Cheng Z: FoxO1 antagonist suppresses autophagy and lipid droplet growth in adipocytes. Cell Cycle. 15:2033–2041. 2016.PubMed/NCBI View Article : Google Scholar | |
Ren H, Shao Y, Wu C, Ma X, Lv C and Wang Q: Metformin alleviates oxidative stress and enhances autophagy in diabetic kidney disease via AMPK/SIRT1-FoxO1 pathway. Mol Cell Endocrinol. 500(110628)2020.PubMed/NCBI View Article : Google Scholar | |
Wang J, Shen L, Hong H, Li J, Wang H and Li X: Atrasentan alleviates high glucose-induced podocyte injury by the microRNA-21/forkhead box O1 axis. Eur J Pharmacol. 852:142–150. 2019.PubMed/NCBI View Article : Google Scholar | |
Guo X, Lin H, Liu J, Wang D, Li D, Jiang C, Tang Y, Wang J, Zhang T, Li Y, et al: 1,25-Dihydroxyvitamin D attenuates diabetic cardiac autophagy and damage by vitamin D receptor-mediated suppression of FoxO1 translocation. J Nutr Biochem. 80(108380)2020.PubMed/NCBI View Article : Google Scholar | |
Sengupta A, Molkentin JD and Yutzey KE: FoxO transcription factors promote autophagy in cardiomyocytes. J Biol Chem. 284:28319–28331. 2009.PubMed/NCBI View Article : Google Scholar | |
Ning Y, Li Z and Qiu Z: FOXO1 silence aggravates oxidative stress-promoted apoptosis in cardiomyocytes by reducing autophagy. J Toxicol Sci. 40:637–645. 2015.PubMed/NCBI View Article : Google Scholar | |
Wang B, Yang Q, Sun YY, Xing YF, Wang YB, Lu XT, Bai WW, Liu XQ and Zhao YX: Resveratrol-enhanced autophagic flux ameliorates myocardial oxidative stress injury in diabetic mice. J Cell Mol Med. 18:1599–1611. 2014.PubMed/NCBI View Article : Google Scholar | |
Li Y, Jiang J, Liu W, Wang H, Zhao L, Liu S, Li P, Zhang S, Sun C, Wu Y, et al: microRNA-378 promotes autophagy and inhibits apoptosis in skeletal muscle. Proc Natl Acad Sci USA. 115:E10849–E10858. 2018.PubMed/NCBI View Article : Google Scholar | |
Yang M, Lin Y and Wang Y and Wang Y: High-glucose induces cardiac myocytes apoptosis through Foxo1 /GRK2 signaling pathway. Biochem Biophys Res Commun. 513:154–158. 2019.PubMed/NCBI View Article : Google Scholar | |
Liu HY, Han J, Cao SY, Hong T, Zhuo D, Shi J, Liu Z and Cao W: Hepatic autophagy is suppressed in the presence of insulin resistance and hyperinsulinemia: Inhibition of FoxO1-dependent expression of key autophagy genes by insulin. J Biol Chem. 284:31484–31492. 2009.PubMed/NCBI View Article : Google Scholar | |
Xiong X, Tao R, DePinho RA and Dong XC: The autophagy-related gene 14 (Atg14) is regulated by forkhead box O transcription factors and circadian rhythms and plays a critical role in hepatic autophagy and lipid metabolism. J Biol Chem. 287:39107–39114. 2012.PubMed/NCBI View Article : Google Scholar | |
Lettieri Barbato D, Tatulli G, Aquilano K and Ciriolo MR: FoxO1 controls lysosomal acid lipase in adipocytes: implication of lipophagy during nutrient restriction and metformin treatment. Cell Death Dis. 4(e861)2013.PubMed/NCBI View Article : Google Scholar : doi.org/10.1038/cddis.2013.404. |